Assessment and conservation status of an endemic bee in a diversity hotspot (Hymenoptera, Melittidae, Dasypoda)

JHR 81: 127-142 (202 I ) ore JOURNAL OF 4 Perreewed openscess oural
doi: 10.3897/jhr.8 1.608 | | RESEARCH ARTICLE () Hymenopter a
https://jhr.pensoft.net Thelnternaonl Society of Hymenopexriss, RESEARCH

Assessment and conservation status of an
endemic bee in a diversity hotspot
(Hymenoptera, Melittidae, Dasypoda)

Guillaume Ghisbain', Vladimir G. Radchenko?, Diego Cejas',

Francisco P. Molina?, Denis Michez!

| Laboratory of Zoology, Research Institute for Biosciences, University of Mons, Place du parc 20, 7000, Mons,
Belgium 2 Institute for Evolutionary Ecology of the National Academy of Sciences of Ukraine, acad. Lebedev,
37, Kiev 03143, Ukraine 3 Departamento de Ecologia Integrativa, Estacién Biolégica de Donana (EBD-
CSIC), Avda. Américo Vespucio S/N Isla de la Cartuja, 41092, Sevilla, Spain

Corresponding author: Guillaume Ghisbain (guillaume.ghisbain@umons.ac.be)

Academic editor: J. Neff | Received 16 November 2020 | Accepted 17 December 2020 | Published 25 February 2021
Attp://zoobank. org/666A641 C-7B44-43 14-8798-7212285B8E8A

Citation: Ghisbain G, Radchenko VG, Cejas D, Molina FP, Michez D (2021) Assessment and conservation status
of an endemic bee in a diversity hotspot (Hymenoptera, Melittidae, Dasypoda). Journal of Hymenoptera Research 81:
127-142. https://doi.org/10.3897/jhr.8 1.60811

Abstract

Wild bees represent a global group of highly diversified insect pollinators, nowadays concerningly well
known for their widespread observed patterns of decline. Amongst them is the genus Dasypoda, a wide-
spread Palearctic clade of solitary bees generally poorly represented in entomological collections. Among the
39 accepted species of the genus, 35 are known by both sexes, and a large number of taxa are still known by
a low number of specimens. The recently described taxon Dasypoda (Heterodasypoda) michezi Radchenko,
2017 endemic to southern Portugal is just such a case. The species was described from two male specimens,
but no female material has been known to date. Here, we provide the first description of the female of D.
michezi, collected close to the locus typicus in southern Portugal along with a series of conspecific males. Sex
pairing is proposed based on the sympatry of the male and female specimens and on the similar morphology
of non-sexual dimorphic traits and on the barcode of a fragment of Cytochrome Oxidase I. We provide high
quality imaging of both sexes of D. michezi to help future identification of the species and present a key for
all known species of the subgenus Heterodasypoda. We finally propose an IUCN status for D. michezi and

discuss the conservation of such geographically restricted species in the current context of global change.

Keywords
Conservation, Dasypoda michezi, endemism, Heterodasypoda, Iberia, IUCN, Portugal, taxonomy

Copyright Guillaume Ghisbain et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

128 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

Introduction

Wild bees constitute a highly diversified group of pollinating insects, comprising more
than 20,000 described species globally (Michener 2007). Approximately a tenth of this
global diversity can be found in Europe, one of the most studied places for bee diver-
sity, biogeography and life history in the world (Michez et al. 2019). Concerningly,
global changes have triggered widespread population declines across several clades of
wild bees, making this group of pollinators widely studied for conservation purposes
(e.g. Potts et al. 2010; Nieto et al. 2014). As for all other animals, nevertheless, the
effective species-level conservation of bees relies on an unambiguous taxonomic deline-
ation and identification. This principle is well exemplified in Red Lists and large-scale
biogeographic studies for which species inventories and occurrence records constitute
the starting point for geographic projections and assessments (Nieto et al. 2014; Ras-
mont et al. 2015; Ghisbain et al. 2020b).

Amongst the bee families represented in Europe is the Melittidae, a species-poor
bee family globally (Michez et al. 2009). Among melittids, the genus Dasypoda Latreille
is remarkable in its unique morphology, specifically by the presence of well-developed
pollen-carrying hair structures (scopae) on the tibia and basitarsus of the hind legs of
the females (Michener 2007; Michez et al. 2019). The genus is predominantly distrib-
uted in the Palearctic region, except for a single sub-Saharan species (Michez and Pauly
2012). To date, 39 valid species are recognized with 35 of them known from both sexes
(Radchenko et al. 2019). Four subgenera are currently recognized within Dasypoda,
with their centers of diversity found in parts of the Mediterranean region: the Balkans,
Morocco and the Iberian Peninsula. Unlike the situation in many groups of wild bees,
there continue to be significant additions to the knowledge of the Dasypoda fauna of
Europe, with the description of new species (Radchenko 2016, 2017) and new records
for many countries (Schmid-Egger and Dubitzky 2017; Ghisbain et al. 2018; Shebl
2018; Radchenko et al. 2019, 2020; Wendzonka et al. 2020).

The most recently described species of the genus, Dasypoda michezi Radchenko,
2017, is a very localized bee known only from two males collected in two nearby locali-
ties in the south-west of Portugal (Radchenko 2017), a biodiversity hotspot for bees
(Baldock et al. 2018). The species belongs to the subgenus Heterodasypoda Michez,
characterized in males by conspicuous morphological autapomorphies, i.e. sternum
7 comprising two large, membranous lateral structures and the genitalia consisting of
three distinct lobes, the inner one with a scaly surface (Michez et al. 2004b). The male
of Dasypoda michezi is distinguishable from its congeners by several features including
the diagnostic sculpture and shape of the glossa, galea and sterna. To date however, the
female of this taxon has not been described (Radchenko 2017).

In this paper, we combine the use of molecular barcoding and the study of mor-
phological traits to provide the first description of the female of Dasypoda michezi. The
description is based on two individuals collected along with a longer set of males in the
south of Portugal, close to the /ocus typicus of the species. We then assess the conserva-
tion status of this overlooked bee species and discuss its conservation as an endemic
bee in a diversity hotspot.

Conservation of an endemic Dasypoda 129

Material and methods

Sampling

We examined a series of Dasypoda (Heterodasypoda) specimens collected in southern
Portugal in the years 2005-2006 by M. and E. Howe, following the taxonomic key
from Michez et al. (2004a). The morphological characteristics of two females could
be identified as those of Heterodasypoda but did not correspond to any previously
known Dasypoda species (following Michez et al. 2004a), while the males could be
determined as Dasypoda michezi Radchenko following the detailed description pro-
vided by Radchenko (2017).

Genetic analyses

We sequenced a fragment of the cytochrome oxidase I (CO/) gene from these two
female specimens and from sympatric males of Dasypoda michezi. DNA was extracted
from a middle leg of every individual using the Nucleo spin Tissue kit (Macherey-
Nagel, Germany) following manufacturer instructions with a lower volume of elution
buffer and expanded final incubation times to improve DNA yield. As pinned speci-
mens from old collections (>10 years) can be difficult to sequence (i.e. their DNA has
degraded over time and moreover is affected by the different processes of preservation
of the collections), it is advisable to amplify small amplicons (<200 bp) (Wandeler et al.
2007). Therefore, modified LEP primers for older samples (LEP-F1/LEP-R2, Hebert
et al. 2004) were selected to amplify a fragment of the cytochrome oxidase subunit 1
(COZ) gene, a region commonly used to study the taxonomic status of animals, and
frequently used in bee taxonomy (e.g. Orr et al. 2018; Weissmann et al. 2018; Ghis-
bain et al. 2020a). After Sanger sequencing (Eurofins Genomics, Spain) and alignment
of the cleaned sequences, we ran a neighbor-joining phylogeny with 10,000 bootstraps
including D. michezi (n = 7, including the two female specimens) along with represent-
atives of each species of Heterodasypoda: D. morotei Quilis, 1928 (n = 2), D. pyrotrichia
Forster, 1855 (n = 1), D. albimana Pérez, 1905 (n = 3). We chose the slightly more
distant Dasypoda (Microdasypoda) crassicornis Friese, 1896 as an outgroup.

Taxonomy

Based on the results of the genetic barcoding (see below), we further examined the
morphology of these females in comparison with that of the males and that of the
other species of Heterodasypoda (i.e. Dasypoda albimana, D. morotei and D. pyrotri-
chia). High-quality pictures of both sexes of D. michezi were taken using a Canon EOS
5DS R (Canon Inc., Tokyo, Japan) camera assembled onto a stereomicroscope Leica
M205C (Leica Microsystems, Wetzlar, Germany) with Leica LED5000 HDI illumina-
tor under Helicon Remote 3.9.7.w. software. Photographs were then combined into
a single image using Helicon Focus 7.5.6 Pro (Helicon Soft Ltd, Kharkiv, Ukraine)

automontage software.

130 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

Finally, we established a key to all known species of Heterodasypoda following
Michez et al. (2004a, b) and the results of the present study. The following abbrevia-
tions, after Michener (2007), are used below: T1, T2... = first, second, etc. metasomal
terga; S1, S2... = first, second, etc. metasomal sterna; Al, A2... = first, second, etc.
antennal segments, pw = puncture width.

Conservation assessment

We assessed an IUCN status for Dasypoda michezi following the Guidelines for using the
IUCN Red List Categories and Criteria V. 14 (https://www.iucnredlist.org/resources/
redlistguidelines) and the protocol of Nieto et al. (2014). To do so, we measured both
the area of occupancy (AOO) and extent of occurrence (EOO) of the species. The
AOO is the measure of the area in which a species occurs and corresponds to the sum
of the area of grids the species occupies, while the EOO is a measure of the geographic
range size of a species and is calculated by drawing a convex hull which is defined as
the smallest polygon containing all the sites of occurrence and in which no internal
angle exceeds 180 °C.

Results

Genetic analyses

The amplified CO/ fragment of the examined male and female specimens of Het-
erodasypoda collected in southern Portugal were identical, and distinct from all
other species of Heterodasypoda (Fig. 1A). Given that the males morphologically
correspond to the original description of Dasypoda (Heterodasypoda) michezi from
Radchenko (2017), we can state with confidence that the examined females belong
to D. michezi. Updated maps of the Western-Mediterranean distributions of the
four known species of Heterodasypoda are given in Figure 1B, C. New sequences
are available on Genbank with the accession numbers MW389319-MW389326;
MW401790-MW401795.

First description of the females of Dasypoda michezi
Figures 2-14

Note. We describe for the first time the female of Dasypoda michezi. Specimens exam-
ined during the study are deposited in the entomological collection of the Laboratory
of Zoology of the University of Mons (Belgium) and in the Institute for Evolutionary
Ecology of the National Academy of Sciences of Ukraine.

Material examined. 2 9, Portugal, Algarve, Sagres Camp/Heath [37.0249°N,
8.9463°W], 13.IV.2006, leg. M. and E. Howe.

Conservation of an endemic Dasypoda 131

D_michezi_Portugal_ female

D_michezi_Portugal_female

D_michezi_Portugal_male
Ci micheri Portusal male Dasypoda michezi Radchenko, 2017

D_michezi_Portugal_male
D_michezi_Portugal_male
D_michezi_Portugal_male
D_albimana_Spain

Dasypoda albimana Pérez, 1905

D. albimana_Spain

D. albimana_Spain

D_pyrotrichia_Spain | Dasypoda pyrotrichia Forster, 1855

D_morotei_Spain ; ons
b, aratel spain Dasypoda morotei Quilis, 1928

| Dasypoda crassicornis Friese, 1896 [OUTGROUP]

D_crassicornis_ Spain

5. oes ot * ates
a. wae f aa ji
- - 7 \ “fp
ati (Ps a 7, a XB Pai t fA s eee, i

Figure |. A CO/ phylogeny of the Heterodasypoda, highlighting the association of both female and male
specimens of D. michezi from southern Portugal, with D. (Microdasypoda) crassicornis as an outgroup
B, C West Mediterranean distribution of the four known species of Heterodasypoda: B records of D. al-
bimana (orange) and D. michezi (red, new records indicated by the black arrow) C records of D. morotei

(green) and D. pyrotrichia (blue). Adapted from Michez et al. (2004) and Radchenko (2017).

Description. Female (Figs 2-15). Body length = 13.5-13.6 mm. Head
(Figs 4-9). W — 3. 55-3.65 mm; H — 3.23—3.25 mm. Face between antennae dull,
densely punctured and bearing erect white and dark (brown-black) hairs, propor-
tion of dark hairs greater on lateral parts of face and just below ocellar field. Area in
front of ocellae very densely punctured and matt, this puncturing less dense behind
ocellar field. Area between lateral ocellae and compound eyes shagreened. Vertex
(Fig. 5) with sparse yellow pilosity and dark erect setae. Clypeus densely punctured,
punctures less than 1 pw apart, on most of its surface, punctures slightly larger and
more separated distally. Medio-distal part of clypeus shiny; distal part with tufts
of short white hair mixed with a few darker setae; hairless medially except in some
areas with a few white and black setae; basal and lateral parts covered with mixed
white and black hairs. Labrum unpunctured and shiny basally; distal part bearing
thick orange setae inserted in large punctures. Mandibles black, in some places with

12 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

Figures 2-14. Female of D. michezi from Algarve, southern Portugal (first description) 2 dorsal view

3 lateral view 4 head (frontal view) 5 vertex and ocelli 6 malar area 7 flagellum and pedicel 8 galea and
maxillary palpus 9 glossa and labial palpus inside the galea (ventral view) 10 scutum I 1 metanotum and

propodeum 12 metasoma (dorsal view) 13 pygidial plate 14 metasoma (ventral view).

dark red shades, bearing long white setae ventrally. Malar space (Fig. 6) shorter than
width of mandible at its base, one specimen bearing very short, thick, white, black
pilosity. Maxillary palpus and galea subequal. Galea with small tubercles merged

Conservation of an endemic Dasypoda Lead

into sinuous lines on most of its surface; margin of galea with bristles all along its
length (Fig. 8). Glossa dark with yellow apical bristles. Maxillary palpi approxi-
mately 0.75 times as long as length of glossa (Fig. 9). Scape with sparse dark or
white setae; surface shiny, sparsely punctate, punctures large. Last article of anten-
nae truncated at apex (Fig. 7).

Mesosoma (Figs 10, 11). W (between tegulae) — 3.15-3.24 mm. Scutum densely
punctured medially (Fig. 10), shagreened between punctures, shiny in center, but matt
laterally. Small unpunctured, shiny area in center of scutum with starting point of
clearly visible carina extending to the most distal part of scutum. Parapsidal lines very
thin and long. Scutum with sparse dark pilosity medially, surrounding parts bearing
erect dark and yellowish pilosity, proportion of yellowish hairs greater laterally. Scutel-
lum, metanotum and propodeum (Fig. 11) densely punctured and matt, scutellum
bearing a majority of erect dark hairs; metanotum and propodeum mostly with yel-
lowish erect setae. Mesosoma ventrally with dense pure-white pilosity ventrally. Tegu-
lae dark brown, slightly shagreened and shiny. Wings transparent, slightly darkened
(Figs 2, 3, 15). Forelegs bearing long brown hairs dorsally, protibia and probasitarsus
with short orange pilosity ventrally. Mesotibia with yellowish-whitish pilosity ventrally
and brown pilosity dorsally. Mesobasitarsus with orange pilosity ventrally, brown pilos-
ity dorsally and whitish pilosity on its outer face. Metatibia and metabasitarsus with
whitish pilosity ventrally and brown pilosity dorsally, metabasitarsus bearing orange
pilosity on its posterior surface.

Metasoma (Figs 12-14). L — 7.7—7.8 mm; W (at widest point) — 4—4.5 mm.
T1 evenly punctate, surface matt, pilosity as on metanotum and propodeum. T2-—
T4 matt and strongly shagreened, bearing whitish tufts of hair laterally, with very
sparse brown pilosity on discs. T'5 with denser and longer erect dark pilosity, except
lateral part with whitish pilosity as on other terga. Punctures of T5 strong, dense,
less than 1 pw apart laterally, but approx. 1 pw medially. Sides of T6 (around py-
gidial plate) bearing the same dense and long dark pilosity as on T5. Pygidial plate
(Fig. 13) hairless, depressed, dark purple, narrowly elongate and bifurcate apically.
Sterna thinly shagreened anteriorly with short brown pilosity, strongly punctured
posteriorly (Fig. 14).

Additional male material examined. Portugal, Algarve, Sagres Camp/Heath
[37.0249°N, 8.9463°W], leg. M and E Howe, 3.IV.2005 (2 33) , 4.1V.2005 (3 43),
7.1V.2005 (1 3) 13.1V.2006 (1 @), at the same place and same day as the presently
described females); 1 <4, Portugal, Algarve, Sagres Campsite [same locality, 37.0249°N,
8.9463°W], 10.IV.2006, leg. M and E Howe; 1 3, Portugal, Algarve, Cabo de Sao
Vicente [37.0227°N, 8.9964°W], 11.IV.2006, leg. M and E Howe. All specimens are
deposited in the Laboratory of Zoology (UMons, Belgium).

Phenology and ecology. Flight period. The previous records of D. michezi were
in late spring (20°—21" May) (Radchenko 2017). Our new records are from earlier in
the season (3'—13" April).

Floral choices. Unfortunately, the labels of the newly recorded specimens do not
carry floral records. Some labels state “Heath”, which may refer to the type of vegeta-
tion at the collecting sites and not the visited plant (Erica).

134 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

Key to the species of Heterodasypoda

Females

1 Pubescence of mesotibia completely white (ventrally and dorsally)................
A sci Upset eeceisa ls vandeetaeetek tig Ras ateaence te onsteleay union taal pte nee Dasypoda albimana

= Pubescence of mesotibia not entirely white, with at least some yellow or
browriishbaits presences. Aart nu decors tO lien com ee ee ae oe ot ecats ve Saat 2

2 Face with entirely black pilosity. Galea with external surface shiny. Scutum cov-

ered with ginger or cream hair. Tegula light orange ....... Dasypoda pyrotrichia
— Pilosity of face including at least some lighter hairs. Galea with external sur-
face either matt or shiny. Scutum with dark pilosity in the center, lighter on
the sides: Lepulatiptowne cmtircttceasecate la Siees ocess cities araietaaet fae ocean tes 3
3 Mesotibia mostly with plumose white pilosity but including coarse spine-like
dark brown hair dorsally (Figs 16-18). Hair band of T4 with sparse, brown
pilosity. Ventral part of mesosoma with white pilosity..... Dasypoda michezi
— Mesotibia with plumose white pilosity but including coarse spine-like yellow
and light brown hair (Figs 19-21). Hair band of T4 wide and dense, medially
white and black on the sides. Ventral part of mesosoma with mixed black and
SFG aW | comm UJ OSI a ae eat a Reece are eects aed ee rate ie ser tee A Dasypoda morotei

Males

Detailed diagnosis of the males of Heterodasypoda is available in Radchenko (2017)
and new pictures of are provided in Figures 22-36.

1 Clypeus-inediallyzcom pletely punctured: 5 2-e cae ac eA ctsael ah olenee de ceet 2
- Clypeus medially with an unpunctured longitudinal carina... eee 3
2 Galea densely covered with wave-like sculptures (Fig. 28). Glossa six times as
long as wide (width taken at its base; Fig. 29) 0... Dasypoda michezi
- Galea with weak inconspicuous sculpting. Glossa three times as long as wide
Gatadthstakeh-atttoujase) ve ce toa teen eee he eee Ne Dasypoda albimana
3 A3 at most as long as A4. S6 deeply indented at the apical margin. Base of
gonostylar internal lobe as wide as external lobe.............. Dasypoda morotei
_ A3 longer than A4. S6 weakly indented at the apical margin. Base of gonosty-
lar internal lobe wider than the external lobe ............. Dasypoda pyrotrichia

Conservation status of Dasypoda michezi

The known EOO of Dasypoda michezi based on all available records encompasses
~199 km? while its known AOO encompasses 16 km? (based on 2 km x 2 km cell
width). Both these measures are associated with the category Endangered following

the IUCN criteria B1 and B2 and their combination with the condition “a” ([Extent/
Habitat] severely fragmented OR |low] number of locations) since the bee has only been

Conservation of an endemic Dasypoda 35

__ 0,1 mm

Figures 15-21. Comparison of the mesotibia pubescence between D. michezi and D. morotei 15 female
of D. michezi (fronto-lateral view; the position of the mesotibia is the same as in Fig. 16) 16-18 pubes-
cence of D. michezi mesotibia under different magnifications 19=21 Pubescence of D. morotei mesotibia

under different magnifications.

136 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

‘ at We
\ Wy N why MN

a | | j ! iil i

Figures 22-36. Male of D. michezi from Algarve, southern Portugal 22 dorsal view 23 lateral view
24 head (frontal view) 25 vertex and ocelli 26 malar area 27 antenna 28 galea and maxillary palpus
29 glossa and labial palpus (dorsal view) 30 scutum 31 propodeum 32 metasoma (dorsal view) 33 metaso-

ma (ventral view) 34 S6-8 and genitalia (ventral view) 35 genitalia (lateral view) 36 genitalia (dorsal view).

Conservation of an endemic Dasypoda iB Es

reported from a very small number of locations. We therefore assess the IUCN Red
List criteria of D. michezi as Endangered with the code B1a+B2a (see discussion).

Discussion

In this work, we provide the first description of the female of Dasypoda michezi, a
poorly known melittid bee endemic to the south of Portugal, and present a key for
both sexes to all known species of the genus Heterodasypoda. We finally assess the con-
servation status of Dasypoda michezi as Endangered at the European scale following the
IUCN protocol. Other known species of the subgenus Heterodasypoda are not under
such threat. In particular, D. albimana is categorized NT, and D. morotei and D. pyro-
trichia LC (Nieto et al. 2014).

Taxonomy

The female of D. michezi presents some singular morphological features compared to
the rest of the Heterodasypoda species, including a clear differentiation in its color pat-
tern from the morphologically closely related D. albimana, the most visible being the
color of the pilosity of the mid-leg (white in D. albimana and dark brown dorsally in
D. michezi). The species confirms the original combination of morphological charac-
teristics of the female sex proposed by Michez et al. (2004) for the subgenus, namely
(i) a clypeus entirely punctured with or without a median carina, (ii) a scopa bicolored,
(iii) the disc of T2 with a rather straight marginal line, (iv) pygidial plate glabrous, (v)
maxillary palpae and galea of a subequal length, (vi) the margin of the galea with setae
along its entire length, (vii) a malar space shorter than the length of the pedicel and
(viii) a prefurcal nervulus.

Ecology and conservation

In a context of global declines in bee populations (Potts et al. 2010), the restricted
distribution of Dasypoda michezi in the south of Portugal ultimately raises questions
about its conservation. Having a restricted distribution implies that, if they occur, all
or most individuals will experience adverse conditions simultaneously (Gaston 1998)
and, because endemic species present by definition a few sites for conservation in-
tervention, they are inherently more vulnerable to extinction in a context of global
changes, particularly climate and habitat change. Moreover, the very recent description
of the species (in 2017) naturally means that it was not attributed to a conservation
status in the Red List of European bees (Nieto et al. 2014). In the latter work, the
subfamily Dasypodainae was amongst the most at risk with 25% of its species being
threatened. The IUCN status assessed here, Endangered with the code Bla + B2a,
closely recalls those of the other threatened Dasypoda that were all assessed at least with
the criterion B2a (accompanied with b[iii]), a threat related to a combination of an
overall small AOO, severely fragmented habitats or a low number of locations, and a

138 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

continuous decline estimated for the quality of the habitat. These criteria are shared
with a large number of other threatened bees in Europe (Nieto et al. 2014), highlight-
ing the need to preserve the most suitable natural habitats for the bee fauna of the con-
tinent (Michez et al. 2019; Ghisbain et al. 2020b). The criterion b(iii), associated with
a continuous decline of habitat quality, is not appropriate for the status of D. michezi
given that the whole known distribution of the species is included in a protected area,
the Parque Natural do Sudoeste Alentejano e Costa Vicentina. Long-term preservation
of such protected habitats is especially critical for bees like Dasypoda due to their rela-
tively specialized foraging behaviour (Michez et al. 2008), a characteristic that could
make them especially susceptible to changes in their environment as they do not switch
to alternative host plants (Scheper et al. 2014). Dasypoda bees rely on flower-rich en-
vironments, and the subgenus Heterodasypoda is mostly associated with Cistaceae and
Asteraceae (Michez et al. 2004b, 2008; Ruiz 2013; Ozbek 2014) with other records on
Lamiaceae and Rosaceae (Michez et al. 2003, 2004b; Ruiz 2013). Radchenko (2017)
highlights the association of the males of D. michezi with Cistus (Cistaceae) pollen,
which is consistent with the floral choices of other representatives of the subgenus.
Further work is needed to characterize in more detail the floral choices of Dasypoda
michezi in this National Park and to estimate the population trends of its host plants in
its restricted range. With global warming and its associated higher intensity of extreme
weather events, such a monitoring of habitat quality is crucial in areas like southern
Portugal where heat waves and fires are already frequent.

In addition to the need to characterize the habitats in which D. michezi occurs,
more observations of the species are also required to precisely delineate the timing of
its flight period. Heterodasypoda bees are known to fly from late spring to late summer:
May-July for D. albimana (Michez et al. 2003), mostly May-August for D. morotei and
D. pyrotrichia (Ornosa and Ortiz-Sanchez 1998, 2004; Grace 2010). Our new records
combined with those of Radchenko (2017) suggest that the flight period of Dasypoda
michezi encompasses April and May (late spring). Overall, given the growing evidence
that significant phenological shifts and mismatches in plant-pollinator interactions
following global warming are occurring (Duchenne et al. 2020; Gérard et al. 2020),
further understanding the species phenology and floral associations during their flight
period is a key to their effective conservation.

Iberian Peninsula as an understudied hotspot of bee diversity

Although Europe constitutes one of the most extensively studied areas in the world for
bees (Michez et al. 2019), the very recent discovery and characterization of Dasypoda
michezi in Portugal is not surprising. New bee species are still continuously described
from the Iberian Peninsula (Miiller 2012; Wood and Cross 2017; Kuhlmann and Smit
2018; Smit 2018; Wood et al. 2020a), a geographic area that constitutes a global hot-
spot not only for bee species diversity (Orr et al. 2020) but also for many other organ-
isms (Gomez and Lunt 2007). In total, over 1000 bee species are known from Spain
(Ortiz-Sanchez 2011, 2020) and 722 from Portugal (Baldock et al. 2018; Wood et al.
2020a). This high diversity is partly due to the role that the Peninsula played as a glacial

Conservation of an endemic Dasypoda 139

refugium during the Quaternary (Hewitt 2011), as well as the Mediterranean climate
of the region, combined with the striking diversity of habitats (i.e. a combination of
meadows, scrublands, mountains, woodlands and coastlines). In particular, the Iberian
Peninsula constitutes a center of diversity for both of the Dasypoda subgenera Micro-
dasypoda and Heterodasypoda. The first subgenus includes four known species, with one
species endemic to Iberia: D. iberica (Michez et al. 2004b; Radchenko et al. 2019). The
second includes four species with two endemics: the currently studied D. michezi and
also D. morotei (Michez et al. 2004b; Radchenko 2017). Despite the extremely rich bee
diversity of the Iberian Peninsula however, both Spain and Portugal present a very high
percentage of species assessed as “data deficient” in the European Red List (Nieto et al.
2014; Wood et al. 2020b). The present case further suggests that additional efforts are
encouraged to characterize and monitor the highly diverse bee fauna of these under-
studied areas. Future projects that focus on understanding the ecology of endemic bee
species and delineating more precisely their distributions are encouraged to assess the
potential threats that these species could face in the near future.

Acknowledgements

The authors are grateful to Thomas J. Wood for helpful comments on the manuscript.
We warmly thank Yulia Astafurova, Ian Cross, Jack Neff and an anonymous reviewer
for their constructive comments and advice on the manuscript. The authors thank
Michael G. Branstetter for kindly helping confirm the CO/ sequences of Dasypoda
morotei. The research leading to this publication received funds from the Fonds de la
Recherche Scientifique-FNRS (Brussels, Belgium) and “The support of the priority
research areas development of Ukraine”, KPKVK 6541230. GG is funded by a ER.S.-
FNRS grant “Aspirant”. DC and DM are partly funded by the ER.S.-FNRS and the
Fonds Wetenschappelijk Onderzoek (FWO) under the EOS project CLIPS (n°3094785).

References

Baldock D, Wood TJ, Cross I, Smit J (2018) The Bees of Portugal. Entomofauna, Supplement
221: 1-164.

Duchenne E Thébault E, Michez D, Elias M, Drake M, Persson M, Rousseau-Piot JS, Pollet
M, Vanormelingen P, Fontaine C (2020) Phenological shifts alter the seasonal structure of
pollinator assemblages in Europe. Nature Ecology and Evolution 4: 115-121. https://doi.
org/10.1038/s41559-019-1062-4

Gérard M, Vanderplanck M, Wood T, Michez D (2020) Global warming and plant-pollina-
tor mismatches. Emerging Topics in Life Sciences 4(1): 77-86. https://doi.org/10.1042/
EELSZOTIOLS9

Ghisbain G, Radchenko VG, Michez D (2018) Dasypoda morawitzi Radchenko 2016 (Apoidea
— Melittidae — Dasypodaini), une espéce nouvelle pour la faune de France. Osmia 7: 10-

13. https://doi.org/10.47446/OSMIA7.2

140 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

Ghisbain G, Lozier JD, Rahman SR, Ezray BD, Tian L, Ulmer JM, Heraghty SD, Strange JP,
Rasmont P, Hines HM (2020a) Substantial genetic divergence and lack of recent gene flow
support cryptic speciation in a colour polymorphic bumble bee (Bombus bifarius) species
complex. Systematic Entomology 45: 635-652. https://doi.org/10.1111/syen.12419

Ghisbain G, Michez D, Marshall L, Rasmont P, Dellicour S (2020b) Wildlife conservation
strategies should incorporate both taxon identity and geographical context — further evi-
dence with bumblebees. Diversity and Distributions 26(12): 1741-1751. https://doi.
org/10.1111/ddi.13155

Goémez A, Lunt D (2007) Refugia within refugia: patterns of phylogeographic concordance in
the Iberian Peninsula. Phylogeography of southern European refugia. Netherlands, Spring-
er, 155-188. https://doi.org/10.1007/1-4020-4904-8_5

Grace A (2010) Introductory biogeography to bees of the Eastern Mediterranean and Near East
(1* Edn.). Bexhill Museum, Bexhill, 284 pp.

Hebert PD, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA
barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.
Proceedings of the National Academy of Sciences of the United States of America 101:
14812-14817. https://doi.org/10.1073/pnas.0406166101

Hewitt GM (2011) Mediterranean Peninsulas: The Evolution of Hotspots. In: Zachos F, Habel
J (Eds) Biodiversity Hotspots. Springer-Verlag Berlin Heidelberg, 123-147. https://doi.
org/10.1007/978-3-642-20992-5_7

Kuhlmann M, Smit J (2018) Description of a new bee species from Spain, Colletes jansmiti
Kuhlmann nov.sp., with a key to the females of the C. albomaculatus-group (Hymenoptera:
Colletidae). Linzer Biologische Beitrage 50: 1249-1254.

Mace GM (2004) The role of taxonomy in species conservation. Philosophical Transactions
of the Royal Society of London. Series B: Biological Sciences 359: 711-719. https://doi.
org/10.1098/rstb.2003.1454

Michener CD (2007) The bees of the world, second edition. The Johns Hopkins University
Press, Baltimore, 953 pp. [20 pls.]

Michez D, Patiny S, Gaspar C (2003) Dasypoda albimana Pérez, 1905 (Hymenoptera, Apoidea,
Melittidae), espéce nouvelle pour la France et le Maroc. Bulletin de la Société ento-
mologique de France 108(1): 61-64.

Michez D, Terzo M, Rasmont P (2004a) Révision des espéces ouest-paléarctiques du genre
Dasypoda Latreille 1802 (Hymenoptera, Apoidea, Melittidae). Linzer biologische Beitrage
36(2): 847-900.

Michez D, Terzo M, Rasmont P (2004b) Phylogénie, biogéographie et choix floraux des abeilles
oligolectiques du genre Dasypoda Latreille 1802 (Hymenoptera: Apoidea: Melittidae). An-
nales de la Société Entomologique de France, New Series 40(3—4): 421-435. https://doi.or
g/10.1080/00379271.2004.10697431

Michez D, Patiny S, Rasmont P, Timmermann K, Vereecken NJ (2008) Phylogeny and host-
plant evolution in Melittidae s./. (Hymenoptera: Apoidea). Apidologie 39(1): 146-162.
https://doi.org/10.1051/apido:2007048

Michez D, Patiny S$, Danforth BN (2009) Phylogeny of the bee family Melittidae (Hyme-
noptera: Anthophila) based on combined molecular and morphological data. Systematic

Entomology 34: 574-597. https://doi.org/10.1111/j.1365-3113.2009.00479.x

Conservation of an endemic Dasypoda 141

Michez D, Pauly A (2012) A new species of the palaearctic genus Dasypoda Latreille 1802
(Hymenoptera: Dasypodaidae) from the Great Rift Valley in Ethiopia. Zootaxa 3181(1):
63-68. https://doi.org/10.11646/zootaxa.3181.1.5

Michez D, Rasmont P, Terzo M, Vereecken NJ (2019) Bees of Europe. Hymenoptera of Europe
(Vol. 1) édition N.A.P., Paris, 552 pp.

Miller A (2012) New European bee species of the tribe Osmiini (Hymenoptera: Apoidea:
Megachilidae). Zootaxa 3355: 29-50. https://doi.org/10.11646/zootaxa.3355.1.2

Nieto A, Roberts SPM, Kemp J, Rasmont P, Kuhlmann M, Garcia Criado M, Biesmeijer JC,
Bogusch P, Dathe HH, De la Ruta P, De Meulemeester T,; Dehon M, Dewulf A, Ortiz-
Sanchez FJ, Lhomme P, Pauly A, Potts SG, Praz C, Quaranta M, Radchenko VG, Scheuchl
E, Smit J, Straka J, Terzo M, Tomozii B, Window J, Michez D (2014) European Red List
of Bees. Publication Office of the European Union, Luxembourg, 98 pp.

Ornosa C, Ortiz-Sanchez FJ (1998) Contribucién al conocimiento de los melitidos ibéricos
(Hymenoptera, Apoidea, Melittidae). Boletin de la Asociacién espafola de Entomologia
22(3—4): 181-202.

Ornosa C, Ortiz-Sanchez FJ (2004) Hymenoptera, Apoidea I. Fauna Ibérica (Vol. 23). In:
Ramos MA, Alba J, Bellés X, Gonsalbes J, Guerra A, Macpherson E, Martin E Serrano J,
Templado J (Eds) Museo Nacional de Ciencias Naturales. CSIC, Madrid, 556 pp.

Ortiz-Sanchez FJ (2011) Lista actualizada de las especies de abejas de Espaha (Hymenoptera:
Apoidea: Apiformes). Boletin de la Sociedad Entomoldgica Aragonesa 49: 265-281.

Ortiz-Sanchez FJ (2020) Checklist de Fauna Ibérica.Serie Anthophila (Insecta: Hymenoptera:
Apoidea) en la peninsula ibérica e islas Baleares (edicibn 2020). In: Ramos MA, Sanchez
Ruiz M (Eds) Documentos Fauna Ibérica, 14. Museo Nacional de Ciencias Naturales,
CSIC. Madrid, [2 (sn)] 83 pp.

Ozbek H (2014) Distribution data on the family Melittidae (Hymenoptera) of Turkey with
considerations about their importance as pollinators. Turkish Journal of Zoology 38: 444—
459. https://doi.org/10.3906/zoo-1309-5

Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pol-
linator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25: 345-353.
https://doi.org/10.1016/j.tree.2010.01.007

Radchenko VG (2016) A new widespread European bee species of the genus Dasypoda Latreille (Hy-
menoptera, Apoidea). Zootaxa 4184(3): 491-504. https://doi.org/10.11646/zootaxa.4184.3.4

Radchenko VG (2017) A new bee species of the genus Dasypoda Latreille (Hymenoptera,
Apoidea) from Portugal with comparative remarks on the subgenus Heterodasypoda Michez.
Zootaxa 4350(1): 164-176. https://doi.org/10.11646/zootaxa.4350.1.10

Radchenko VG, Ghisbain G, Michez D (2019) Redescription of three rare species of Dasypoda
bees with first description of D. iberica and D. tibialis females (Hymenoptera, Apoidea,
Melittidae). Zootaxa 4700: 326-344. https://doi.org/10.11646/zootaxa.4700.3.2

Radchenko VG, Tomozii B, Ghisbain G, Michez D (2020) New data on the morphology
and distribution of the cryptic species Dasypoda morawitzi Radchenko 2016 (Hymenop-
tera: Melittidae) with corrections of Dasypoda s. str. diagnosis. Annales de la Société Ento-
mologique de France (N.S.). https://doi.org/10.1080/00379271.2020.1841570

Rasmont P, Franzen M, Lecocq T, Harpke A, Roberts S, Biesmeijer K, Castro L, Cederberg B,
Dvorak L, Fitzpatrick U, Gonseth Y, Haubruge E, Mahe G, Manino A, Michez D, Neu-

142 Guillaume Ghisbain et al. / Journal of Hymenoptera Research 81: 127-142 (2021)

mayer J, Odegaard EF, Paukkunen J, Pawlikowski T, Potts S, Reemer M, Settele J, Straka
J, Schweiger O (2015) Climatic Risk and Distribution Atlas of European Bumblebees.
BioRisk 10: 1-236. https://doi.org/10.3897/biorisk.10.4749

Ruiz JL (2013) Fuentes alimenticias de los Melittidae ibéricos. Micobotanica-Jaén 8(3): 18-22.

Scheper J, Reemer M, van Kats R, Ozinga WA, van der Linden GTJ, Schaminee JHJ, Siepel H,
Kleijn D (2014) Museum specimens reveal loss of pollen host plants as key factor driving
wild bee decline in The Netherlands. Proceedings of the National Academy of Sciences
111(49): 17552-17557. https://doi.org/10.1073/pnas. 1412973111

Wandeler P, Hoeck PE, Keller LF (2007) Back to the future: museum specimens in population
genetics. Trends in Ecology and Evolution 22(12): 634-642. https://doi.org/10.1016/j.
tree.2007.08.017

Weissmann JA, Picancgo A, Borges PAV, Schaefer H (2017) Bees of the Azores: an annotated
checklist (Apidae, Hymenoptera). ZooKeys 642: 63-95. https://doi.org/10.3897/zook-
eys.642.10773

Wendzonka J, Celary W, Klejdysz T, Krzysztofiak A, Pawlikowski T, Postowska J, Rutkowski
T, Twerd L, Zurawlew P (2020) Dasypoda morawitzi Radchenko 2016 (Hymenoptera,
Apoidea) a new species in the Polish fauna. Ampulex 11: 5-8.

Wood TJ, Cross I (2017) Camptopoeum (Camptopoeum) baldocki spec. nov., a new panurgine
bee species from Portugal and a description of the male of Flavipanurgus fuzetus Pat-
iny (Andrenidae: Panurginae). Zootaxa 4254(2): 285-293. https://doi.org/10.11646/
zootaxa.4254.2.9

Wood TJ, Cross I, Baldock D (2020a) Updates to the bee fauna of Portugal with the descrip-
tion of three new Iberian Andrena species (Hymenoptera: Apoidea: Anthophila). Zootaxa
4790(2): 201-228. https://doi.org/10.11646/zootaxa.4790.2.1

Wood T, Michez D, Paxton R, Drossart M, Neumann P, Gerard M, Vanderplanck M, Barraud
A, Martinet B, Leclercq N, Vereecken NJ (2020b) Managed honey bees as a radar for wild
bee decline? Apidologie 51: 1100-1116. https://doi.org/10.1007/s13592-020-00788-9